The synergistic action of melittin and phospholipase A2 with lipid membranes: Development of linear dichroism for membrane-insertion kinetics

Protein and Peptide Letters

Volumn 17, Issue 11, 2010, Pages 1351-1362

  Damianoglou, Angeliki ^a   Rodger, Alison ^a   Pridmore, Catherine ^b   Dafforn, Timothy R ^c   Mosely, Jackie A ^b   Sanderson, John M ^b   Hicks, Matthew R ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Amphipathic; Antimicrobial; Dynamic light scattering; Linear dichroism; Liposome; Membrane protein; Peptide

Indexed keywords

APOIDEA;

EID: 78649798863     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/0929866511009011351     Document Type: Article

References (54)

1. Wallin, E.; von Heijne, G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci., 1998, 7, 1029-1038
2. Terstappen, G. C.; Reggiani, A. In silico research in drug discovery. Trends Pharmacol. Sci., 2001, 22, 23-26
3. Vaara, M. New approaches in peptide antibiotics. Curr. Opin. Pharmacol., 2009, 9, 571-576
4. Hancock, R. E. W.; Chappel, D. S. Peptide antibiotics. Antimicrob. Agents Chemother., 1999, 43(6), 1317-1323
5. Ardhammar, M.; Mikati, N.; Norden, B. Chromophore orientation in liposome membranes probed with flow linear dichroism. J. Am. Chem. Soc., 1998, 720, 9957-9958
6. Rajendra, J.; Baxendale, M.; Dit Rap, L. G.; Rodger, A. Flow linear dichroism to probe binding of aromatic molecules and DNA to single walled carbon nanotubes. J. Am. Chem. Soc., 2004, 726, 11182-11188.
7. Rajendra, J.; Damianoglou, A.; Hicks, M.; Booth, P.; Rodger, P. M.; Rodger, A. Quantitation of protein orientation in flow-oriented unilamellar liposomes by linear dichroism. Chem. Phys., 2006, 326(1), 210-220.
8. Ennaceur, S. M.; Hicks, M. R.; Pridmore, C. J.; Dafforn, T. R.; Rodger, A.; Sanderson, J. M. Peptide adsorption to lipid bilayers Slow rearrangement processes revealed by linear dichroism spectroscopy. Biophys. J., 2009, 96(4), 1399-1407
9. Esbjorner, E. K.; Caesar, C. E. B.; Albinsson, B.; Lincoln, P.; Norden, B. Tryptophan orientation in model lipid membranes. Biochem. Biophys. Res. Commun., 2007, 361, 645-650
10. Esbjorner, E. K.; Oglcka, K.; Lincoln, P.; Graslund, A.; Norden, B. Membrane binding of ph-sensitive influenza fusion peptides. Positioning, configuration, and induced leakage in a lipid vesicle model. Biochemistry, 2007, 46, 13490-13504
11. Hicks, M. R.; Dafforn, T.; Damianoglou, A.; Wormell, P.; Rodger, A.; Hoffmann, S. V. Synchrotron radiation linear dichroism spectroscopy of the antibiotic peptide gramicidin in lipid membranes. Analyst, 2009, 134, 1623-1628
12. Hicks, M. R.; Damianoglou, A.; Rodger, A.; Dafforn, T. R. Folding and membrane insertion of the pore-forming peptide gramicidin occur as a concerted process. J. Mol. Biol., 2008, 383(2), 358-66
13. Raghuraman, H.; Chattopadhyay, A. Melittin: a membrane-active peptide with diverse functions. Biosci. Rep., 2007, 27, 189-223
14. Talbot, J. C. Conformational change and self association of monomeric melittin. FEBS Lett., 1979, 102, 191-193
15. Dempsey, C. E. The actions of melittin on membranes. Biochim. Biophys. Acta, 1990, 1031, 143-161
16. Shai, Y. Molecular recognition between membrane-spanning polypeptides. Trends Biochem. Sci., 1995, 20, 460-464
17. Papo, N.; Shai, Y. Exploring peptide membrane interaction using surface plasmon resonance: Differentiation between pore formation versus membrane disruption by lytic peptides. Biochemistry, 2003, 42, 458-466.
18. Bogaart, G. v. d.; Guzman, J. V.; Mika, J. T.; Poolman, B. On the mechanism of pore formation by melittin. J. Biol. Chem., 2008, 283, 33854-33857.
19. Manna, M.; Mukhopadhyay, C. Cause and effect of melittin-induced pore formation: A computational approach. Langmuir, 2009, 25, 12235-12242.
20. Casey, D. R.; Sebai, S. C.; Shearman, G. C.; Ces, O.; Law, R. V.;Gee, A. D.; Templer, R. H. Formulation affects the rate of membrane degradation catalyzed by cationic amphiphilic drugs. Ind. Eng. Chem. Res., 2008, 47, 650-665
21. Dempsey, C. E.; Watts, A. A. Deuterium and phosphorus-31 nuclear magnetic resonance study of the interaction of melittin with dmpc bilayers and the effects of contaminating phospholipase a2. Biochemistry, 1987, 26, 5803-5811.
22. Marrington, R.; Dafforn, T. R.; Halsall, D. J.; Hicks, M.; Rodger, A. Validation of new microvolume couette flow linear dichroism cells. Analyst, 2005, 130, 1608-1616
23. Marrington, R.; Dafforn, T. R.; Halsall, D. J.; Rodger, A. Micro volume couette flow sample orientation for absorbance and fluorescence linear dichroism. Biophys. J., 2004, 87, 2002-2012
24. Rodger, A.; Marrington, R.; Geeves, M. A.; Hicks, M.; de Alwis, L.; Halsall, D. J.; Dafforn, T. R. Looking at long molecules in solution: What happens when they are subjected to couette flow? Phys. Chem. Chem. Phys., 2006, 8(27), 3161-3171.
25. Rodger, A.; Patel, K. K.; Sanders, K. J.; Datt, M.; Sacht, C.; Hannon, M. J. Anti-tumour platinum acylthiourea complexes and their interactions with DNA. Dalton, 2002, 3656-3663
26. Rodger, A.; Rajendra, J.; Marrington, R.; Ardhammar, M.; Norden, B.; Hirst, J. D.; Gilbert, A. T. B.; Dafforn, T. R.; Halsall, D. J.; Woolhead, C. A.; Robinson, C.; Pinheiro, T. J.; Kazlauskaite, J.; Seymour, M.; Perez, N.; Hannon, M. J. Flow oriented linear dichroism to probe protein orientation in membrane environments. Phys. Chem. Chem. Phys., 2002, 4, 4051-4057.
27. Andersson, A.; Biverstahl, H.; Nordin, J.; Lindahl, E.; Maler, L. The membrane induced structure of melittin is correlated with the fluidity of the lipids. Biochim. Biophys. Acta, 2007, 1768, 115-121
28. Constantinescu, I.; Lafleur, M. Influence of the lipid composition on the kinetics of concertedinsertion and folding of melittin in bilayers. Biochim. Biophys. Acta, 2004, 1667, 26-37.
29. Ghosh, A. K.; Rukmini, R.; Chattopadhyay, A. Modulation of tryptophan environment in membrane-bound melittin by negatively charged phospholipids: Implications in membrane organization and function, . Biochemistry, 1997, 36, 14291-14305.
30. Raghuraman, H.; Chattopadhyay, A. Interactions of melittin with membrane cholesterol: A fluorescence approach. Biophys. J., 2004, 87, 2419-2432. (Pubitemid 41071340)
31. Sui, S. Conformational changes of melittin upon insertion into phospholipid monolayer and vesicle. J. Biochem., 1994, 116, 482 487.
32. Veen, M. V.; Georgiou, G. N.; Drake, A. F.; Cherry, R. J. Circular-dichroism and fluorescence studies on melittin: Effects of c-terminal modifications on tetramer formation and binding to phospholipid vesicles. Biochem. J., 1995, 305, 785-790.
33. Ladokhin, A. S.; White, S. H. Folding of amphipathic alpha-helices on membranes: Energetics of helix formation by melittin. J. Mol. Biol., 1999, 285, 1363-1369.
34. Lazarova, T.; Brewin, K. A.; Stoeber, K.; Robinson, C. R. Characterization of peptides corresponding to the seven transmembrane domains of human adenosine a2a receptor. Biochemistry, 2004, 43, 12945-12954.
35. Thevenin, D.; Lazarova, T.; Roberts, M. F.; Robinson, C. R. Oligomerization of the fifth transmembrane domain from the adenosine a2a receptor. Protein Sci., 2005, 14, 2177-2186.
36. Raghuraman, H.; Chattopadhyay, A. Influence of lipid chain unsaturation on membrane bound melittin : a fluorescence approach. Biochim. Biophys. Acta, 2004, 1665, 29-39.
37. Norden, B.; Rodger, A.; Dafforn, T. Linear dichroism and circular dichroism: A textbook on polarized-light spectroscopy. Royal Society of Chemistry: Cambridge, 2010.
38. Apitz-Castro, R.; Jain, M. K.; De Haas, G. H. Origin of the latency phase during the action of phospholipase a2 on unmodified phosphatidylcholine vesicles. Biochim. Biophys. Acta, 1982, 688(2), 349-56.
39. Bell, J. D.; Burnside, M.; Owen, J. A.; Royall, M. L.; Baker, M. L. Relationships between bilayer structure and phospholipase a2 activity: Interactions among temperature, diacylglycerol, lysolecithin, palmitic acid, and dipalmitoylphosphatidylcholine. Biochemistry, 1996, 35(15), 4945-55.
40. Op den Kamp, J. A.; Kauerz, M. T.; van Deenen, L. L. Action of pancreatic phospholipase a2 on phosphatidylcholine bilayers in different physical states. Biochim. Biophys. Acta, 1975, 406(2), 169-77.
41. Wells, M. A. Mechanism of interfacial activation of phospholipase a2. Biochemistry, 1974, 13(11), 2248-2257
42. Code, C.; Domanov, Y. A.; Killian, J. A.; Kinnunen, P. K. Activation of phospholipase a2 by temporin b: Formation of antimicrobial peptide-enzyme amyloid-type cofibrils. Biochim. Biophys. Acta, 2009, 1788(5), 1064-72
43. Koumanov, K.; Momchilova, A.; Wolf, C. Bimodal regulatory effect of melittin and phospholipase a2-activating protein on human type ii secretory phospholipase a2. Cell Biol. Int., 2003, 27(10), 871-7.
44. Mingarro, I.; Perez-Paya, E.; Pinilla, C.; Appel, J. R.; Houghten, R. A.; Blondelle, S. E. Activation of bee venom phospholipase a2 through a peptide-enzyme complex. FEBS Lett., 1995, 372(1), 1314.
45. Pochet, S.; Tandel, S.; Querriere, S.; Tre-Hardy, M.; Garcia Marcos, M.; De Lorenzi, M.; Vandenbranden, M.; Marino, A.; Devleeschouwer, M.; Dehaye, J. P. Modulation by ll-37 of the responses of salivary glands to purinergic agonists. Mol. Pharmacol., 2006, 69(6), 2037-46.
46. Signor, G.; Mammi, S.; Peggion, E.; Ringsdorf, H.; Wagenknecht, A. Interaction of bombolitin iii with phospholipid monolayers and liposomes and effect on the activity of phospholipase a2. Biochemistry, 1994, 33(21), 6659-70.
47. Zhao, H.; Kinnunen, P. K. Modulation of the activity of secretory phospholipase a2 by antimicrobial peptides. Antimicrob. Agents Chemother., 2003, 47(3), 965-71
48. Thuren, T.; Tulkki, A. P.; Virtanen, J. A.; Kinnunen, P. K. Triggering of the activity of phospholipase a2 by an electric field. Biochemistry, 1987, 26(16), 4907-10
49. Dufton, M. J.; Hider, R. C.; Cherry, R. J. The influence of melittin on the rotation of band 3 protein in the human erythrocyte membrane. Eur. Biophys. J., 1984, 11(1), 17-24
50. Rudenko, S. V.; Nipot, E. E. Protection by chlorpromazine, albumin and bivalent cations against haemolysis induced by melittin, [ala-14]melittin and whole bee venom. Biochem. J., 1996, 317 (Pt 3), 747-54
51. Mitchell, D. C. Molecular order and dynamics in bilayers consisting of highly polyunsaturated phospholipids. Biophys. J., 1998, 74, 879-891.
52. Saiz, L. Computer simulation studies of model biological membranes. Acc. Chem. Res., 2002, 35, 482-489.
53. Baciu, M.; Sebai, S. C.; Ces, O.; Mulet, X.; Clarke, J. A.; Shearman, G. C.; Law, R. V.; Templer, R. H.; Plisson, C.; Parker, C. A.; Gee, A. Degradative transport of cationic amphiphilic drugs across phospholipid bilayers. Philos. Trans. R. Soc., A, 2006, 364, 2597-2614
54. Shearman, G. C.; Attard, G. S.; Hunt, A. N.; Jackowski, S.; Baciu, M.; Sebai, S. C.; Mulet, X.; Clarke, J. A.; Law, R. V.; Plisson, C.; Parker, C. A.; Gee, A.; Ces, O.; Templer, R. H. Using membrane stress to our advantage. Biochem. Soc. Trans., 2007, 35, 498-501.